Neural basis of shape representation in the primate brain.

Visual shape recognition--the ability to recognize a wide variety of shapes regardless of their size, position, view, clutter and ambient lighting--is a remarkable ability essential for complex behavior. In the primate brain, this depends on information processing in a multistage pathway running from primary visual cortex (V1), where cells encode local orientation and spatial frequency information, to the inferotemporal cortex (IT), where cells respond selectively to complex shapes. A fundamental question yet to be answered is how the local orientation signals (in V1) are transformed into selectivity for complex shapes (in IT). To gain insights into the underlying mechanisms we investigated the neural basis of shape representation in area V4, an intermediate stage in this processing hierarchy. Theoretical considerations and psychophysical evidence suggest that contour features, i.e. angles and curves along an object contour, may serve as the basis of representation at intermediate stages of shape processing. To test this hypothesis we studied the response properties of single units in area V4 of primates. We first demonstrated that V4 neurons show strong systematic tuning for the orientation and acuteness of angles and curves when presented in isolation within the cells' receptive field. Next, we found that responses to complex shapes were dictated by the curvature at a specific boundary location within the shape. Finally, using basis function decoding, we demonstrated that an ensemble of V4 neurons could successfully encode complete shapes as aggregates of boundary fragments. These findings identify curvature as a basis of shape representation in area V4 and provide insights into the neurophysiological basis for the salience of convex curves in shape perception.

[1]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[2]  Azriel Rosenfeld,et al.  From volumes to views: An approach to 3-D object recognition , 1992, CVGIP Image Underst..

[3]  A. Cowey,et al.  On the role of cortical area V4 in the discrimination of hue and pattern in macaque monkeys , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Ravi S. Menon,et al.  An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings , 2000, Current Biology.

[5]  R. von der Heydt,et al.  Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  D. W. Heeley,et al.  Mechanisms Specialized for the Perception of Image Geometry , 1996, Vision Research.

[7]  S. Ullman Aligning pictorial descriptions: An approach to object recognition , 1989, Cognition.

[8]  Donald D. Hoffman,et al.  Parts of Visual Objects: An Experimental Test of the Minima Rule , 1989, Perception.

[9]  J. Baizer,et al.  Visual responses of area 18 neurons in awake, behaving monkey. , 1977, Journal of neurophysiology.

[10]  K Tanaka,et al.  Neuronal mechanisms of object recognition. , 1993, Science.

[11]  Ichiro Fujita,et al.  Disparity-selective neurons in area V4 of macaque monkeys. , 2002 .

[12]  P. H. Schiller,et al.  The role of the primate extrastriate area V4 in vision. , 1991, Science.

[13]  D. Marr,et al.  Representation and recognition of the spatial organization of three-dimensional shapes , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[14]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[15]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[16]  Nathan Intrator,et al.  Towards structural systematicity in distributed, statically bound visual representations , 2003, Cogn. Sci..

[17]  J. Maunsell,et al.  Visual effects of lesions of cortical area V2 in macaques , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  H. Komatsu,et al.  Influence of the Direction of Elemental Luminance Gradients on the Responses of V4 Cells to Textured Surfaces , 2001, The Journal of Neuroscience.

[19]  Charles E Connor,et al.  Quantitative characterization of disparity tuning in ventral pathway area V4. , 2005, Journal of neurophysiology.

[20]  Whitman Richards,et al.  Attentional frames, frame curves and figural boundaries: The inside/outside dilemma , 1996, Vision Research.

[21]  Leslie G. Ungerleider,et al.  Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques , 1996, Visual Neuroscience.

[22]  P. Lennie Receptive fields , 2003, Current Biology.

[23]  I. Biederman Recognition-by-components: a theory of human image understanding. , 1987, Psychological review.

[24]  R Vogels,et al.  Macaque inferior temporal neurons are selective for disparity-defined three-dimensional shapes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Dennis M. Levi,et al.  Angle judgment: Is the whole the sum of its parts? , 1996, Vision Research.

[26]  D. Regan,et al.  Evidence for a neural mechanism that encodes angles , 1996, Vision Research.

[27]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[28]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[29]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[30]  Rufin Vogels,et al.  Processing of kinetic boundaries in macaque V4. , 2006, Journal of neurophysiology.

[31]  E. Rolls,et al.  View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. , 1998, Cerebral cortex.

[32]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[34]  Ramesh C. Jain,et al.  Three-dimensional object recognition , 1985, CSUR.

[35]  I. Biederman,et al.  Priming contour-deleted images: Evidence for intermediate representations in visual object recognition , 1991, Cognitive Psychology.

[36]  F. Attneave Some informational aspects of visual perception. , 1954, Psychological review.

[37]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[38]  D. P. Andrews,et al.  Acuities for spatial arrangement in line figures: human and ideal observers compared. , 1973, Vision research.

[39]  Charles E Connor,et al.  Underlying principles of visual shape selectivity in posterior inferotemporal cortex , 2004, Nature Neuroscience.

[40]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[41]  Keiji Tanaka,et al.  Coding visual images of objects in the inferotemporal cortex of the macaque monkey. , 1991, Journal of neurophysiology.

[42]  David L. Sheinberg,et al.  Visual object recognition. , 1996, Annual review of neuroscience.

[43]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[44]  G. Orban,et al.  Responses of visual cortical neurons to curved stimuli and chevrons , 1990, Vision Research.

[45]  Hugh R. Wilson,et al.  Non-Fourier Cortical Processes in Texture, Form, and Motion Perception , 1999 .

[46]  C. Connor,et al.  Population coding of shape in area V4 , 2002, Nature Neuroscience.

[47]  Nathan Intrator,et al.  (coarse Coding of Shape Fragments) (retinotopy) Representation of Structure , 2000 .

[48]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[49]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[50]  C. Connor,et al.  Three-dimensional orientation tuning in macaque area V4 , 2002, Nature Neuroscience.

[51]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[53]  D H HUBEL,et al.  RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT. , 1965, Journal of neurophysiology.

[54]  S Edelman,et al.  (Coarse coding of shape fragments) + (retinotopy) approximately = representation of structure. , 2000, Spatial vision.

[55]  Minami Ito,et al.  Size and position invariance of neuronal responses in monkey inferotemporal cortex. , 1995, Journal of neurophysiology.

[56]  R. Desimone,et al.  Visual areas in the temporal cortex of the macaque , 1979, Brain Research.

[57]  Jay Hegdé,et al.  Role of primate visual area V4 in the processing of 3-D shape characteristics defined by disparity. , 2005, Journal of neurophysiology.

[58]  R. Vogels,et al.  Inferotemporal neurons represent low-dimensional configurations of parameterized shapes , 2001, Nature Neuroscience.

[59]  Alex Pentland,et al.  Shape Information From Shading: A Theory About Human Perception , 1988, [1988 Proceedings] Second International Conference on Computer Vision.

[60]  Takahiro Doi,et al.  Disparity-tuning characteristics of neuronal responses to dynamic random-dot stereograms in macaque visual area V4. , 2005, Journal of neurophysiology.

[61]  J. Gallant The Neural Representation of Shape , 2000 .

[62]  Donald D. Hoffman,et al.  Parts of recognition , 1984, Cognition.

[63]  I. Fujita,et al.  Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex , 2000, Nature Neuroscience.

[64]  Hong Zhou,et al.  Representation of stereoscopic edges in monkey visual cortex , 2000, Vision Research.

[65]  J. Gallant,et al.  A Human Extrastriate Area Functionally Homologous to Macaque V4 , 2000, Neuron.

[66]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[67]  G. Orban,et al.  Cue-invariant shape selectivity of macaque inferior temporal neurons. , 1993, Science.

[68]  C. Connor,et al.  Shape representation in area V4: position-specific tuning for boundary conformation. , 2001, Journal of neurophysiology.

[69]  M. Behrmann,et al.  Impact of learning on representation of parts and wholes in monkey inferotemporal cortex , 2002, Nature Neuroscience.

[70]  P. H. Schiller Effect of lesions in visual cortical area V4 on the recognition of transformed objects , 1995, Nature.

[71]  Steven W. Zucker,et al.  Two Stages of Curve Detection Suggest Two Styles of Visual Computation , 1989, Neural Computation.

[72]  P. Milner A model for visual shape recognition. , 1974, Psychological review.

[73]  W. Merigan,et al.  Basic visual capacities and shape discrimination after lesions of extrastriate area V4 in macaques , 1996, Visual Neuroscience.

[74]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.

[75]  P. Hammond,et al.  Collinearity tolerance of cells in areas 17 and 18 of the cat's visual cortex: Relative sensitivity to straight lines and chevrons , 1978, Experimental Brain Research.

[76]  J. Hegdé,et al.  Selectivity for Complex Shapes in Primate Visual Area V2 , 2000, The Journal of Neuroscience.

[77]  Minami Ito,et al.  Representation of Angles Embedded within Contour Stimuli in Area V2 of Macaque Monkeys , 2004, The Journal of Neuroscience.

[78]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[79]  Leslie G. Ungerleider,et al.  Contour, color and shape analysis beyond the striate cortex , 1985, Vision Research.

[80]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[81]  S. Zucker,et al.  Endstopped neurons in the visual cortex as a substrate for calculating curvature , 1987, Nature.

[82]  H. Wilson,et al.  Concentric orientation summation in human form vision , 1997, Vision Research.

[83]  P. Heggelund,et al.  Responses of striate cortical cells to moving edges of different curvatures , 1975, Experimental Brain Research.

[84]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[85]  I. Biederman,et al.  Dynamic binding in a neural network for shape recognition. , 1992, Psychological review.

[86]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[87]  J M Wolfe,et al.  Curvature is a Basic Feature for Visual Search Tasks , 1992, Perception.

[88]  T. Poggio,et al.  A network that learns to recognize three-dimensional objects , 1990, Nature.

[89]  P. Rakic,et al.  Modulation of neuronal migration by NMDA receptors. , 1993, Science.

[90]  E. Iwai,et al.  Responsiveness of inferotemporal single units to visual pattern stimuli in monkeys performing discrimination , 1980, Experimental Brain Research.

[91]  H. A. Pham,et al.  V4 lesions in macaques affect both single- and multiple-viewpoint shape discriminations , 1998, Visual Neuroscience.

[92]  D. C. Essen,et al.  Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. , 1996, Journal of neurophysiology.

[93]  S. Ullman Three-dimensional object recognition based on the combination of views , 1998, Cognition.

[94]  N. Sigala,et al.  Visual categorization shapes feature selectivity in the primate temporal cortex , 2002, Nature.

[95]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[96]  Y. Yamane,et al.  Complex objects are represented in macaque inferotemporal cortex by the combination of feature columns , 2001, Nature Neuroscience.

[97]  Walter Gerbino,et al.  Convexity and Symmetry in Figure-Ground Organization , 1976 .